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References

  1. Beuchat LR, Kim H, Gurtler JB, Lin LC, Ryu JH, Richards GM. 2009. Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. Int. J. Food Microbiol. 136: 204-213.
    Pubmed CrossRef
  2. Blazkova M, Javurkova B, Fukal L, Rauch P. 2011. Immunochromatographic strip test for detection of genus Cronobacter. Biosens. Bioelectron. 26: 2828-2834.
    Pubmed CrossRef
  3. Bochot A, Fattal E. 2012. Liposomes for intravitreal drug delivery: a state of the art. J. Control. Release 161: 628-634.
    Pubmed CrossRef
  4. Bowen AB, Braden CR. 2006. Invasive Enterobacter sakazakii disease in infants. Emerg. Infect. Dis. 12: 1185-1189.
    Pubmed PMC CrossRef
  5. Chap J, Jackson P, Siqueira R, Gaspar N, Quintas C, Park J, et al. 2009. International survey of Cronobacter sakazakii and other Cronobacter spp. in follow up formulas and infant foods. Int. J. Food Microbiol. 136: 185-188.
    Pubmed CrossRef
  6. Chen F, Ming X, Chen X, Gan M, Wang B. 2014. Immunochromatographic strip for rapid detection of Cronobacter in powdered infant formula in combination with silica-coated magnetic nanoparticles separation and 16S rRNA probe. Biosens. Bioelectron. 61: 306-313.
    Pubmed CrossRef
  7. DeCory TR, Durst RA, Zimmerman SJ, Garringer LA, Paluca C, Decory HK, et al. 2005. Development of an immunomagnetic bead immunoliposome fluorescence assay for rapid detection of Escherichia coli O157:H7 in aqueous samples and comparison of the assay with a standard microbiological method. Appl. Environ. Microbiol. 71: 1856-1864.
    Pubmed PMC CrossRef
  8. Food and Agriculture Organization of the United Nations (FAO)/World Health Organization (WHO). 2006. Enterobacter sakazakii and Salmonella in powdered infant formula: meeting report. World Health Organization, Genenva.
  9. Food and Agriculture Organization of the United Nations (FAO)/World Health Organization (WHO). 2007. Guidelines:safe preparation, storage and handling of powdered infant formula. World Health Organization, Genenva.
  10. Gallova J, Uhrikova D, Islamov A, Kuklin A. 2004. Effect of cholesterol on the bilayer thickness in unilamellar extruded DLPC and DOPC liposome: SANS contrast variation study. Gen. Physiol. Biophys. 13: 113-128.
  11. Gomez-Hens A, Fernadez-Romero JMF. 2005. The role of liposomes in analytical processes. Trends Anal. Chem. 24: 9-19.
    CrossRef
  12. Ho JA, Zeng SC, Tseng WH, Lin YJ, Chen CH. 2008. Liposome-based immunostrip for the rapid detection of Salmonella. Anal. Bioanal. Chem. 391: 479-485.
    Pubmed CrossRef
  13. Holy O, Forsythe S. 2014. Cronobacter spp. as emerging causes of healthcare-associated infection. J. Hosp. Infect. 86:169-177.
    Pubmed CrossRef
  14. Iversen C, Forsythe S. 2003. Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends Food Sci. Technol. 14: 443-454.
    CrossRef
  15. Iversen C, Forsythe S. 2004. Isolation of Enterobacter sakazakii and other Enterobacteriaceae from powdered infant milk and related products. Food Microbiol. 21: 771-777.
    CrossRef
  16. Iversen C, Lehner A, Mullane N, Bidlas E, Cleenwerck I, Marugg J, et al. 2007. The taxonomy of Enterobacter sakazakii:proposal of a new genus Cronobacter gen. nov. and descriptions of Cronobacter sakazakii comb. nov., Cronobacter sakazakii subsp. sakazakii, comb. nov., Cronobacter sakazakii subsp. malonaticus subsp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov. and Cronobacter genomospecies. BMC Evol. Biol. 7: 64.
    Pubmed PMC CrossRef
  17. Iversen C, Mullane N, McCardell B, Tall BD, Lehner A, Fanning S, et al. 2008. Cronobacter gen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov. comb. nov., C. malonaticus sp. nov., C. turicensis sp. nov., C. muytjensii sp. nov., C. dublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies, C. dublinensis sp. nov. subsp. dublinensis subsp. nov., C. dublinensis sp. nov. subsp. lausannensis subsp. nov., and C. dublinensis sp. nov. subsp. lactaridi subsp. nov. Int. J. Syst. Evol. Microbiol. 58: 1442-1447.
    Pubmed CrossRef
  18. Jackson EE, Sonbol H, Masood N, Forsythe SJ. 2014. Reevaluation of a suspected Cronobacter sakazakii outbreak in Mexico. Food Microbiol. 44: 226-235.
    Pubmed CrossRef
  19. Jesorka A, Orwar O. 2008. Liposomes: technologies and analytical applications. Annu. Rev. Anal. Chem. 1: 801-832.
    Pubmed CrossRef
  20. Joseph S, Cetinkaya E, Drahovska H, Levican A, Figueras MJ, Forsythe S. 2012. Cronobacter condimenti sp. nov., isolated from spiced meat and Cronobacter universalis sp. nov., a novel species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water, and food ingredients. Int. J. Syst. Evol. Microbiol. 62: 1277-1283.
    Pubmed CrossRef
  21. Jung MK, Park JH. 2006. Prevalence and thermal stability of Enterobacter sakazakii from unprocessed ready-to-eat agricultural products and powdered infant formulas. Food Sci. Biotechnol. 15: 152-157.
  22. Kim H, Beauchat LR. 2005. Survival and growth of Enterobacter sakazakii on fresh-cut fruits and vegetables and in unpasteurized juices as affected by storage temperature. J. Food Protect. 68: 2541-2552.
    Pubmed
  23. Lee YD, Park JH, Chang H. 2012. Detection, antibiotic susceptibility and biofilm formation of Cronobacter spp. from various foods in Korea. Food Control 24: 225-230.
    CrossRef
  24. Shukla S, Bang J, Heu S, Kim M. 2012. Development of immunoliposome-based assay for the detection of Salmonella Typhimurium. Eur. Food Res. Technol. 234: 53-59.
    CrossRef
  25. Shukla S, Lee G, Song X, Park S, Kim M. 2016. Immunoliposome-based immunomagnetic concentration and separation assay for rapid detection of Cronobacter sakazakii. Biosens. Bioelectron. 77: 986-994.
    Pubmed CrossRef
  26. Shukla S, Lee H, Kim M. 2011. Development of a liposomebased immunochromatographic strip assay for the detection of Salmonella. Anal. Bioanal. Chem. 401: 2581-2590.
    Pubmed CrossRef
  27. Shukla S, Leem H, Lee J, Kim M. 2014. Immunochromatographic strip assay for the rapid and sensitive detection of Salmonella Typhimurium in artificially contaminated tomato samples. Can. J. Microbiol. 60: 399-406.
    Pubmed CrossRef
  28. Song C, Li J, Liu J, Liu Q. 2016. Simple sensitive rapid detection of Escherichia coli O157:H7 in food sample by label-free immunofluorescence strip sensor. Talanta 156-157:42-47.
    Pubmed CrossRef
  29. Song X, Shukla S, Oh S, Kim Y, Kim M. 2015. Development of fluorescence-based liposome immunoassay for detection of Cronobacter muytjensii in pure culture. Curr. Microbiol. 70: 246-252.
    Pubmed CrossRef
  30. Stephan R, Grim CJ, Goponath GR, Mammel MK, Sathyamorrthy V, Trach LH, et al. 2014. Re-examination of the taxonomic status of Enterobacter helveticus, Enterobacter pulveris and Enterobacter turicensis as members of the genus Cronobacter and their reclassification in the genera Franconibacter gen. nov. and Siccibacter gen. nov. as Franconibacter helveticus comb. nov., Franconibacter pulveris comb. nov. and Siccibacter turicensis comb. nov., respectively. Int. J. Syst. Evol. Microbiol. 64: 3402-3410.
    Pubmed PMC CrossRef
  31. Sun Y, Wang M, Liu H, Wang J, He X, Zeng J, et al. 2011. Development of an O-antigen serotyping scheme for Cronobacter sakazakii. Appl. Environ. Microbiol. 77: 2209-2014.
    Pubmed PMC CrossRef
  32. Torchilin VP. 2005. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 4: 145-160.
    Pubmed CrossRef
  33. US Food and Drug Administration. 2002. US Food and Drug Administration website. http://www.fda.gov/Food/ScienceResearch/LaboratoryMethods/ucm114665.htm.
  34. van Acker J, de Smet F, Muyldermans G, Bougatef A, Naessens A, Lauwers S. 2001. Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. J. Clin. Microbiol. 39: 293-297.
    Pubmed PMC CrossRef
  35. Wang X, Zhu CQ, Xu XL, Zhou GH. 2012. Real-time PCR with internal amplification control for the detection of Cronobacter spp. (Enterobacter sakazakii) in food samples. Food Control 25: 144-149.
    CrossRef
  36. World Health Organization. 2004. Enterobacter sakazakii and other microorganisms in powdered infant formula: meeting report. World Health Organization, Geneva.
  37. World Health Organization. 2007. Enterobacter sakazakii and Salmonella in powdered infant formula. World Health Organization, Geneva.
  38. Xu X, Li C, Wu Q, Zhang J, Huang J, Yang G. 2015. Prevalence, molecular characterization, and antibiotic susceptibility of Cronobacter spp. in Chinese ready-to-eat foods. Int. J. Food Microbiol. 204: 17-23.
    Pubmed CrossRef
  39. Zhao Y, Yao Y, Xiao M, Lee CC, Zhang L, Zhang KX, et al. 2013. Rapid detection of Cronobacter sakazakii in dairy food by biofunctionalized magnetic nanoparticle based on nuclear magnetic resonance. Food Control 34: 436-443.
    CrossRef
  40. Zhu S, Schnell S, Matthias F. 2012. Rapid detection of Cronobacter spp. with a method combining impedance technology and rRNA based lateral flow assay. Int. J. Food Microbiol. 159: 54-58.
    Pubmed CrossRef
  41. Zimmermann J, Schmidt H, Loessener MJ, Weiss A. 2014. Development of a rapid detection system for opportunistic pathogenic Cronobacter spp. in powdered milk products. Food Microbiol. 42: 19-25.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(11): 1855-1862

Published online November 28, 2016 https://doi.org/10.4014/jmb.1606.06004

Copyright © The Korean Society for Microbiology and Biotechnology.

Immunochromatographic Strip Assay for Detection of Cronobacter sakazakii in Pure Culture

Xinjie Song 1, Shruti Shukla 1, Gibaek Lee 1 and Myunghee Kim 1*

Department of Food Science and Technology, Yeungnam University, Gyeongsan 38541, Republic of Korea

Received: June 3, 2016; Accepted: July 26, 2016

Abstract

Cronobacter sakazakii (C. sakazakii) is a foodborne pathogen, posing a high risk of disease to
infants and immunocompromised individuals. In order to develop a quick, easy, and sensitive
assay for detecting C. sakazakii, a rabbit anti-C. sakazakii immunoglobulin G (IgG) was
developed using sonicated cell protein from C. sakazakii. The developed anti-C. sakazakii (IgG)
was of good quality and purity, as well as species-specific. The developed rabbit anti-C.
sakazakii IgG was attached to the surface of a sulforhodamine B-encapsulated liposome to form
an immunoliposome. A test strip was then prepared by coating goat anti-rabbit IgG onto the
control line and rabbit anti-C. sakazakii IgG onto the test line, respectively, of a plastic-backed
nitrocellulose membrane. A purple color signal both on the test line and the control line
indicated the presence of C. sakazakii in the sample, whereas purple color only on the control
line indicated the absence of C. sakazakii in the sample. This immunochromatographic strip
assay could produce results in 15 min with a limit of detection of 107 CFU/ml in C. sakazakii
culture. The immunochromatographic strip assay also showed very good specificity without
cross-reactivity with other tested Cronobacter species. Based on these results, the developed
immunochromatographic strip assay is efficient for the detection of C. sakazakii and has high
potential for on-site detection.

Keywords: Antibody, Cronobacter sakazakii, immunochromatographic strip assay, liposome, rapid detection

References

  1. Beuchat LR, Kim H, Gurtler JB, Lin LC, Ryu JH, Richards GM. 2009. Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. Int. J. Food Microbiol. 136: 204-213.
    Pubmed CrossRef
  2. Blazkova M, Javurkova B, Fukal L, Rauch P. 2011. Immunochromatographic strip test for detection of genus Cronobacter. Biosens. Bioelectron. 26: 2828-2834.
    Pubmed CrossRef
  3. Bochot A, Fattal E. 2012. Liposomes for intravitreal drug delivery: a state of the art. J. Control. Release 161: 628-634.
    Pubmed CrossRef
  4. Bowen AB, Braden CR. 2006. Invasive Enterobacter sakazakii disease in infants. Emerg. Infect. Dis. 12: 1185-1189.
    Pubmed KoreaMed CrossRef
  5. Chap J, Jackson P, Siqueira R, Gaspar N, Quintas C, Park J, et al. 2009. International survey of Cronobacter sakazakii and other Cronobacter spp. in follow up formulas and infant foods. Int. J. Food Microbiol. 136: 185-188.
    Pubmed CrossRef
  6. Chen F, Ming X, Chen X, Gan M, Wang B. 2014. Immunochromatographic strip for rapid detection of Cronobacter in powdered infant formula in combination with silica-coated magnetic nanoparticles separation and 16S rRNA probe. Biosens. Bioelectron. 61: 306-313.
    Pubmed CrossRef
  7. DeCory TR, Durst RA, Zimmerman SJ, Garringer LA, Paluca C, Decory HK, et al. 2005. Development of an immunomagnetic bead immunoliposome fluorescence assay for rapid detection of Escherichia coli O157:H7 in aqueous samples and comparison of the assay with a standard microbiological method. Appl. Environ. Microbiol. 71: 1856-1864.
    Pubmed KoreaMed CrossRef
  8. Food and Agriculture Organization of the United Nations (FAO)/World Health Organization (WHO). 2006. Enterobacter sakazakii and Salmonella in powdered infant formula: meeting report. World Health Organization, Genenva.
  9. Food and Agriculture Organization of the United Nations (FAO)/World Health Organization (WHO). 2007. Guidelines:safe preparation, storage and handling of powdered infant formula. World Health Organization, Genenva.
  10. Gallova J, Uhrikova D, Islamov A, Kuklin A. 2004. Effect of cholesterol on the bilayer thickness in unilamellar extruded DLPC and DOPC liposome: SANS contrast variation study. Gen. Physiol. Biophys. 13: 113-128.
  11. Gomez-Hens A, Fernadez-Romero JMF. 2005. The role of liposomes in analytical processes. Trends Anal. Chem. 24: 9-19.
    CrossRef
  12. Ho JA, Zeng SC, Tseng WH, Lin YJ, Chen CH. 2008. Liposome-based immunostrip for the rapid detection of Salmonella. Anal. Bioanal. Chem. 391: 479-485.
    Pubmed CrossRef
  13. Holy O, Forsythe S. 2014. Cronobacter spp. as emerging causes of healthcare-associated infection. J. Hosp. Infect. 86:169-177.
    Pubmed CrossRef
  14. Iversen C, Forsythe S. 2003. Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends Food Sci. Technol. 14: 443-454.
    CrossRef
  15. Iversen C, Forsythe S. 2004. Isolation of Enterobacter sakazakii and other Enterobacteriaceae from powdered infant milk and related products. Food Microbiol. 21: 771-777.
    CrossRef
  16. Iversen C, Lehner A, Mullane N, Bidlas E, Cleenwerck I, Marugg J, et al. 2007. The taxonomy of Enterobacter sakazakii:proposal of a new genus Cronobacter gen. nov. and descriptions of Cronobacter sakazakii comb. nov., Cronobacter sakazakii subsp. sakazakii, comb. nov., Cronobacter sakazakii subsp. malonaticus subsp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov. and Cronobacter genomospecies. BMC Evol. Biol. 7: 64.
    Pubmed KoreaMed CrossRef
  17. Iversen C, Mullane N, McCardell B, Tall BD, Lehner A, Fanning S, et al. 2008. Cronobacter gen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov. comb. nov., C. malonaticus sp. nov., C. turicensis sp. nov., C. muytjensii sp. nov., C. dublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies, C. dublinensis sp. nov. subsp. dublinensis subsp. nov., C. dublinensis sp. nov. subsp. lausannensis subsp. nov., and C. dublinensis sp. nov. subsp. lactaridi subsp. nov. Int. J. Syst. Evol. Microbiol. 58: 1442-1447.
    Pubmed CrossRef
  18. Jackson EE, Sonbol H, Masood N, Forsythe SJ. 2014. Reevaluation of a suspected Cronobacter sakazakii outbreak in Mexico. Food Microbiol. 44: 226-235.
    Pubmed CrossRef
  19. Jesorka A, Orwar O. 2008. Liposomes: technologies and analytical applications. Annu. Rev. Anal. Chem. 1: 801-832.
    Pubmed CrossRef
  20. Joseph S, Cetinkaya E, Drahovska H, Levican A, Figueras MJ, Forsythe S. 2012. Cronobacter condimenti sp. nov., isolated from spiced meat and Cronobacter universalis sp. nov., a novel species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water, and food ingredients. Int. J. Syst. Evol. Microbiol. 62: 1277-1283.
    Pubmed CrossRef
  21. Jung MK, Park JH. 2006. Prevalence and thermal stability of Enterobacter sakazakii from unprocessed ready-to-eat agricultural products and powdered infant formulas. Food Sci. Biotechnol. 15: 152-157.
  22. Kim H, Beauchat LR. 2005. Survival and growth of Enterobacter sakazakii on fresh-cut fruits and vegetables and in unpasteurized juices as affected by storage temperature. J. Food Protect. 68: 2541-2552.
    Pubmed
  23. Lee YD, Park JH, Chang H. 2012. Detection, antibiotic susceptibility and biofilm formation of Cronobacter spp. from various foods in Korea. Food Control 24: 225-230.
    CrossRef
  24. Shukla S, Bang J, Heu S, Kim M. 2012. Development of immunoliposome-based assay for the detection of Salmonella Typhimurium. Eur. Food Res. Technol. 234: 53-59.
    CrossRef
  25. Shukla S, Lee G, Song X, Park S, Kim M. 2016. Immunoliposome-based immunomagnetic concentration and separation assay for rapid detection of Cronobacter sakazakii. Biosens. Bioelectron. 77: 986-994.
    Pubmed CrossRef
  26. Shukla S, Lee H, Kim M. 2011. Development of a liposomebased immunochromatographic strip assay for the detection of Salmonella. Anal. Bioanal. Chem. 401: 2581-2590.
    Pubmed CrossRef
  27. Shukla S, Leem H, Lee J, Kim M. 2014. Immunochromatographic strip assay for the rapid and sensitive detection of Salmonella Typhimurium in artificially contaminated tomato samples. Can. J. Microbiol. 60: 399-406.
    Pubmed CrossRef
  28. Song C, Li J, Liu J, Liu Q. 2016. Simple sensitive rapid detection of Escherichia coli O157:H7 in food sample by label-free immunofluorescence strip sensor. Talanta 156-157:42-47.
    Pubmed CrossRef
  29. Song X, Shukla S, Oh S, Kim Y, Kim M. 2015. Development of fluorescence-based liposome immunoassay for detection of Cronobacter muytjensii in pure culture. Curr. Microbiol. 70: 246-252.
    Pubmed CrossRef
  30. Stephan R, Grim CJ, Goponath GR, Mammel MK, Sathyamorrthy V, Trach LH, et al. 2014. Re-examination of the taxonomic status of Enterobacter helveticus, Enterobacter pulveris and Enterobacter turicensis as members of the genus Cronobacter and their reclassification in the genera Franconibacter gen. nov. and Siccibacter gen. nov. as Franconibacter helveticus comb. nov., Franconibacter pulveris comb. nov. and Siccibacter turicensis comb. nov., respectively. Int. J. Syst. Evol. Microbiol. 64: 3402-3410.
    Pubmed KoreaMed CrossRef
  31. Sun Y, Wang M, Liu H, Wang J, He X, Zeng J, et al. 2011. Development of an O-antigen serotyping scheme for Cronobacter sakazakii. Appl. Environ. Microbiol. 77: 2209-2014.
    Pubmed KoreaMed CrossRef
  32. Torchilin VP. 2005. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 4: 145-160.
    Pubmed CrossRef
  33. US Food and Drug Administration. 2002. US Food and Drug Administration website. http://www.fda.gov/Food/ScienceResearch/LaboratoryMethods/ucm114665.htm.
  34. van Acker J, de Smet F, Muyldermans G, Bougatef A, Naessens A, Lauwers S. 2001. Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. J. Clin. Microbiol. 39: 293-297.
    Pubmed KoreaMed CrossRef
  35. Wang X, Zhu CQ, Xu XL, Zhou GH. 2012. Real-time PCR with internal amplification control for the detection of Cronobacter spp. (Enterobacter sakazakii) in food samples. Food Control 25: 144-149.
    CrossRef
  36. World Health Organization. 2004. Enterobacter sakazakii and other microorganisms in powdered infant formula: meeting report. World Health Organization, Geneva.
  37. World Health Organization. 2007. Enterobacter sakazakii and Salmonella in powdered infant formula. World Health Organization, Geneva.
  38. Xu X, Li C, Wu Q, Zhang J, Huang J, Yang G. 2015. Prevalence, molecular characterization, and antibiotic susceptibility of Cronobacter spp. in Chinese ready-to-eat foods. Int. J. Food Microbiol. 204: 17-23.
    Pubmed CrossRef
  39. Zhao Y, Yao Y, Xiao M, Lee CC, Zhang L, Zhang KX, et al. 2013. Rapid detection of Cronobacter sakazakii in dairy food by biofunctionalized magnetic nanoparticle based on nuclear magnetic resonance. Food Control 34: 436-443.
    CrossRef
  40. Zhu S, Schnell S, Matthias F. 2012. Rapid detection of Cronobacter spp. with a method combining impedance technology and rRNA based lateral flow assay. Int. J. Food Microbiol. 159: 54-58.
    Pubmed CrossRef
  41. Zimmermann J, Schmidt H, Loessener MJ, Weiss A. 2014. Development of a rapid detection system for opportunistic pathogenic Cronobacter spp. in powdered milk products. Food Microbiol. 42: 19-25.
    Pubmed CrossRef